Diversity and Distribution of Orchid Bees (Hymenoptera: Apidae) with a Revised Checklist of Species
←
→
Page content transcription
If your browser does not render page correctly, please read the page content below
874 November - December 2007
SYSTEMATICS, MORPHOLOGY AND PHYSIOLOGY
Diversity and Distribution of Orchid Bees (Hymenoptera: Apidae) with a
Revised Checklist of Species
ANDRÉ NEMÉSIO AND FERNANDO A. SILVEIRA
Lab. Sistemática e Ecologia de Abelhas,Depto. Zoologia – ICB – Univ. Federal de Minas Gerais,
C. postal 486, 30.123-970, Belo Horizonte, MG, andre@nemesio.com.br or andre.nemesio@gmail.com
Neotropical Entomology 36(6):874-888 (2007)
Diversidade e Distribuição de Abelhas Euglossinas (Hymenoptera: Apidae), com uma Lista Revisada de
Espécies
RESUMO - O objetivo do presente estudo foi investigar os padrões de distribuição e diversidade das
abelhas euglossinas (Euglossina). Análises de agrupamento e de correlação foram aplicados a dados
extraídos de 28 levantamentos de euglossinas na Região Neotropical. Os 28 sítios de coleta agruparam-
se em três regiões biogeográficas principais que, de forma geral, correspondem à Bacia Amazônica,
à Mata Atlântica e à América Central. As três áreas, assim como as sub-regiões de cada uma delas,
coincidem, em geral, com os componentes biogeográficos identificados para outras abelhas e organismos
com base em análises filogenéticas. A Floresta Amazônica, como um todo, apresentou a fauna mais
rica e os mais elevados índices de endemismo. A Mata Atlântica, por outro lado, apresentou a fauna
mais pobre e os mais baixos índices de endemismo. No entanto, há que se destacar que um importante
bioma neotropical, o cerrado, é praticamente desconhecido no que diz respeito à sua fauna de abelhas
euglossinas. Pelo menos 30% das espécies listadas são endêmicas de cada bioma. Uma lista atualizada
das espécies de Euglossina é apresentada.
PALAVRAS-CHAVE: Amazônia, Mata Atlântica, Região Neotropical, conservação, taxonomia
ABSTRACT - The aim of this study was to investigate the diversity and distribution patterns of orchid
bees (Euglossina). Cluster and correlation analyses were applied to data extracted from 28 orchid-
bee surveys throughout the Neotropical Region. The 28 sampling sites were grouped in three main
biogeographic areas that roughly correspond to the Amazonian Basin, the Atlantic Forest and Central
America. These three regions, as well as subregions within each of them, correspond approximately to
biogeographic components identified through phylogeny-based analyses for other bees and organisms.
The Amazonian Forest as a whole has the richest fauna and the highest levels of endemism. The Atlantic
Forest, on the other hand, showed the poorest fauna and the lowest levels of endemism. However,
a major neotropical biome, in which orchid bees are known to occur, has not been sampled yet, the
savanna-like cerrado. At least 30% of the species are endemic to each biome. An updated checklist of
the species of Euglossina is provided.
KEY WORDS: Amazon, Atlantic Forest, conservation, Neotropics, taxonomy
Consideration of broad geographic patterns is critical 1982). Since aromatic compounds attractive to orchid bees were
to conceptual development and empirical evaluation of discovered in the 1960’s (Dodson et al. 1969), several inventories
hypotheses in ecology, as well as in conservation and have been carried out in an attempt to characterize the local
evolutionary biology. Documenting the way in which faunas of these bees. Differences in sampling methodology,
diversity differs across a given region and understanding the however, require care to be taken when comparison among
mechanisms that produce such variation are critical steps in local samples is attempted, as noted by Morato (1998) and
the design of regional (and global) conservation strategies and Nemésio & Morato (2004, 2006). Methodological variations
the implementation of regional management plans (Lyons & involved include diversity of chemical baits employed; duration
Willig 2002). of seasonal and daily sampling periods and whether bees are
Orchid bees [Hymenoptera: Apidae: Apini: Euglossina trapped or hand-netted. Moreover, in some cases, bees were
(following the proposition of Roig-Alsina in Roig-Alsina identified in the field but not collected.
& Michener 1993)] frequently are the only pollinators of In spite of these problems, much data have become
hundreds of plant species in the Neotropics (revised by Dressler available in the last 35 years and an attempt to characterize theNovember - December 2007 Neotropical Entomology 36(6) 875
regional faunas of orchid bees should be made. Nevertheless, the cluster analyses described below were extracted from
since there are no hypotheses for the phylogenetic many surveys conducted by several researchers across the
relationships among the species of most orchid-bee genera, Neotropical Region (Fig. 1). To reach a reasonable degree
and no such hypothesis will be achieved soon, no historical of standardization, the data were selected according to the
analysis of orchid bee distribution can be attempted at the following criteria: (i) we used only results from surveys in
moment. The aim of this paper, thus, was to employ the which male orchid bees were attracted to aromatic baits
available data on orchid bee distributions in a descriptive (collected using bait traps and insect nets, or attracted but
analysis, to gain a better understanding of their patterns of not collected); (ii) the number of specimens (or percentage)
geographic distribution. of each orchid bee species collected in the area had to be
available, since they are necessary for cluster analyses. Thus,
simple lists indicating presence/absence were not considered;
Material and Methods (iii) cineole (or eucalyptol), one of the most attractive baits,
had to be used; (iv) at least two of the following five baits
Distribution patterns for orchid bees were searched in had to be used in addition to cineole: vanillin, benzyl acetate,
two ways. First, data obtained from a set of local orchid methyl salicylate, eugenol, and skatole. The use of at least two
bee surveys were employed in cluster analyses to delimit of these baits together with cineole would make it possible to
biogeographic regions based on faunistic similarity of attract a high percentage of the orchid bee species occurring
sites across the Neotropics. After this, all known orchid- in a given site (e. g. Rebêlo & Garófalo 1997, Morato et al.
bee species were assigned to the regions identified above, 1992, Bezerra & Martins 2001); (v) for most studies, when
according to their known geographic distributions, so that more then one site was sampled in the same region, the
regional species-richness and endemism rates could be results of all samples were pooled together and the average
compared. In preparing the data matrix and a check list frequency of these regional samples was employed in the
of orchid bee species (Appendix 1), a series of taxonomic analyses. Exceptions to these were the two sites at Tambopata
decisions had to be made. The problems encountered and the Reserve, Peru (Pearson & Dressler 1985), three Costa Rican
way they were dealt with are explained in Appendix 1. sites (Janzen et al. 1982), and two sites in northeastern
state of São Paulo, Brazil (Rebêlo & Garófalo 1997), due
Data basis of local orchid bee faunas. Data employed in to the differences in habitat, elevation or to long distances
80°W 70°W 60°W 50°W 40°W
10°N CR2, CR3 PAN 10°N
CR1
0°N 0°N
AM1, AM2, AM3, AM4 MA3
MA4 MA1
MA2
PB
10°S 10°S
BA2
PE1, PE2
BA1
BH1, BH2 EMG ES
20°S 20°S
SP2 RSC
SMG
SP1, SP3 RJ
1:27,000,000
0 250 500 1000 RS
30°S km 30°S
80°W 70°W 60°W 50°W 40°W
Fig. 1. Sampling sites for Euglossina, which data were employed in this study. Data from the multiple sites in Rio Grande do
Sul state (RS), Brazil, were merged. Codes of the areas are given in the text and in Table 1.876 Nemésio & Silveira - Diversity and Distribution of Orchid Bees (Hymenoptera: Apidae) with a Revised...
between sites. On the other hand, in the state of Rio Grande Based on these similarities, the areas were grouped using
do Sul (Wittmann et al. 1988), several sites were sampled UPGMA (Sneath & Sokal 1973). Two sets of data were used:
in different parts of the state (see Fig. 1), but only the total (i) all the orchid bee species, and (ii) only Euglossa species.
data were presented. In one case (Oliveira & Campos 1996), For Rio Grande do Sul, Brazil, only data for all orchid bee
in which two sites were sampled for both the understory species were used, since only seven individuals of Euglossa
and canopy, the sites were pooled; however, data from the were caught, four of which were not identified to species
canopy and understory were considered separate from each level (Wittmann et al. 1988).
other. This was done to check the degree of distinctiveness
between understory and canopy faunas, when data from all Checklist of orchid bee species. The known geographic
the Neotropical Region were considered. Data from all other distribution of each valid species of Euglossina was established
sites employed in our study pertain to understory orchid bee through the available literature and included as Appendix 1.
fauna. The species are organized there according to their occurrence
The selected studies were: Janzen et al. (1982) and in the three major regions defined by the analyses described
Ackerman (1983), for Evergreen Tropical Forests in Central above: Atlantic Forest (including the Subtropical Rain Forest
America; Pearson & Dressler (1985), Becker et al. (1991), of southern Brazil, the Semideciduous Atlantic Forest in the
Morato et al. (1992), and Oliveira & Campos (1996), for interior of the states of São Paulo and Minas Gerais, and some
the Amazonian Forest; Wittmann et al. (1988) for the other vegetational types within the Atlantic Forest domain,
Subtropical Atlantic Forest of the state of Rio Grande do such as the mangrove area in southern Bahia); Amazon
Sul, Brazil; Rebêlo & Garófalo (1991, 1997), for the semi- Forest (including parts of northern South America – the so-
deciduous Atlantic Forest of northeastern region of the called Venezuelan Corridor, and Peruvian and Ecuadorian
state of São Paulo, Brazil; Bonilla-Gómez (1999) for the areas east to the Andes); and Central America (including the
Atlantic Rain Forest in the Reserva Florestal de Linhares, Caribbean islands, northern Colombia, Mexico and southern
in the state of Espírito Santo, Brazil; Peruquetti et al. United States). These are not homogeneous areas and include
(1999) for the seasonal semi-deciduous Atlantic Forest different areas of endemism within their limits, such as the
of Viçosa, southeastern Minas Gerais, Brazil; Nemésio Panamanian Endemic Zone (Kimsey 1982), which is included
& Silveira (2007) for four fragments of semi-deciduous in the Central American region (see also Amorim & Pires
Atlantic Forest in Belo Horizonte, state of Minas Gerais, 1996, Camargo 1996, Camargo & Pedro 2003). In general,
Brazil; Nemésio (2004) for nine Atlantic Forest fragments however, these divisions represented areas of relatively high
around Belo Horizonte and three sites in the Atlantic Forest similarity (see results) and are generally coincident with
of the Reserva Particular do Patrimônio Natural da Serra do biogeographic areas delimited through phylogeny-based
Caraça, central Minas Gerais, Brazil; Nemésio & Silveira analyses of data obtained for other groups of animals (see
(2006) for a large remnant of semi-deciduous Atlantic Forest, Discussion). In addition to these three major regions, species
the Parque Estadual do Rio Doce, Eastern Minas Gerais, common to two adjacent areas (Atlantic Forest and Amazon
Brazil; Tonhasca Jr. et al. (2002) for the Atlantic Rain Forest Basin or Amazon Basin and Central America) were treated
of the Desengano region, state of Rio de Janeiro, Brazil; separately. Pan-neotropical species, species with disjunct
Bezerra & Martins (2001), for the Atlantic Rain Forest of geographic distributions, and species endemic to other
the state of Paraíba, Brazil; Neves & Viana (1997) for a biomes were also included in Appendix 1.
mangrove area in southern state of Bahia, Brazil; Neves
& Viana (1999) for a gallery forest immersed in a caatinga
matrix in northern Bahia, Brazil; Rebêlo & Cabral (1997) Results
for a western coastal lowland zone in the state of Maranhão,
Brazil; Silva & Rebêlo (1999) for Amazonia in the state of Faunistic regions. When the 28 study areas were grouped
Maranhão, Brazil; Silva & Rebêlo (2002) for Cajual Island, according to the similarity of their orchid bee faunas (Figs.
Maranhão, Brazil; and Brito & Rêgo (2001) for a secondary 2 and 3), the sites within the Atlantic Forest domain were
forest in Alcântara, Maranhão, Brazil (see Fig. 1 for exact clustered separately from the sites within the Amazonian
localization of the areas and Table 1 for acronyms used in Forest domain. These groupings were similar both when
this paper). all Euglossina and when only species of Euglossa were
considered. When all Euglossina were included in the
Cluster analysis. Similarity between all site-pairs was analysis, part of the Central American fauna grouped with
calculated using the frequency of each species in the selected the Amazonian fauna, but part of the fauna from Costa
samples. The percent similarity-index of Renkonen was Rica (Parque Nacional Santa Rosa) was quite distinct from
employed for this calculation. According to Wolda (1981), the other regions (Fig. 2). However, when only Euglossa
when small samples are compared, this index is relatively were included in the analysis, the Central-American local
insensitive to sample size and species diversity, as compared faunas clustered together as one distinct group (Fig. 3). The
to other similarity indexes. Moreover, it has other desirable position of the Alcântara area (in the northeastern Brazilian
characteristics – (i) only presence of common species adds state of Maranhão – MA4) also changed depending on the
up to the similarity between two sites and (ii) the contribution data set employed in the analysis. When all Euglossina were
of any given species to the total similarity can be readily considered, Alcântara clustered with the Atlantic Forest areas,
accessed, being equal to its minimum observed frequency albeit with low similarity; when only species of Euglossa
in the two sites compared. were considered, it clustered with the Amazonian region,November - December 2007 Neotropical Entomology 36(6) 877
Table 1. Number of bees and species, sampling method, chemical baits used and frequency of the commonest orchid
bee species in 28 areas in the Neotropics.
No.
Areas Authors No. bees Method1 Baits2
species
Rio Grande do Sul - RS Wittmann et al. (1988) 639 5 IN C, SK, V
Rebêlo & Garófalo
Faz. Santa Carlota (SS) – SP1 892 8 IN C, E, V
(1991)
Rebêlo & Garófalo
EEZ – SP2 736 10 IN C, E, V
(1997)
Rebêlo & Garófalo
Faz. Santa Carlota (SI) – SP3 906 14 IN C, E, V
(1997)
Viçosa – SMG Peruquetti et al. (1999) 893 10 BT AB, C, E, SM, V
Nemésio & Silveira
Belo Horizonte 1997 – BH1 1,325 14 IN AB, C, CM, E, V
(2007)
Belo Horizonte 1999 – BH2 Nemésio (2004) 2,146 14 IN AB, C, CM, E, V
Res. Serra do Caraça - RSC Nemésio (2004) 236 10 IN AB, C, CM, E, V
Parque Estadual Rio Doce – Nemésio & Silveira AB, BI, BM, BZ, C, CM,
1,183 18 IN
EMG (2006) CR, DB, E, SK, SM, T, V
Tonhasca Jr. et al.
Rio de Janeiro – RJ 3,653 21 IN C, CM, E, SK, SM, V
(2002)
Espírito Santo – ES Bonilla-Gómez (1999) 16,177 31 OBS C, E, SM, SK, V
Mangrove Bahia – BA1 Neves & Viana (1997) 1,144 12 BT C, E, SM, V
Gallery Forest – BA2 Neves & Viana (1999) 527 7 IN+BT BB, C, CM, E, V
Bezerra & Martins
Paraíba – PB 1,082 9 BT AA, AB, C, E, SM, V
(2001)
Lowland Coast. zone – MA1 Rebêlo & Cabral (1997) 1,153 9 IN BB, C, E, SM
Buriticupu – MA2 Silva & Rebêlo (1999) 1,740 37 IN BB, C, E, SM, V
Cajual Island – MA3 Silva & Rebêlo (2002) 339 19 IN C, E, SM, V
Alcântara – MA4 Brito & Rêgo (2001) 467 19 IN BB, C, E, SM, V
Amazon 1991 – AM1 Becker et al. (1991) 290 16 BT C, SK, SM
Amazon 1992 – AM2 Morato et al. (1992) 1,242 27 IN AB, C, E, SM
Amazon 1996 understory – Oliveira & Campos AB, BB, C, CM, E, SK,
1,145 33 BT
AM3 (1996) SM, V
Oliveira & Campos AB, BB, C, CM, E, SK,
Amazon 1996 canopy – AM4 1,277 35 BT
(1996) SM, V
AA, AB, AC, AlB, C, CM,
Pearson & Dressler
Peru – Floodplain – PE1 1,178 183 IN dC, E, EC, pC, pCy, pE, Pi,
(1985)
SK, SM, V
AA, AB, AC, AlB, C,
Pearson & Dressler
Peru – Terra Firme – PE2 1,661 183 IN CM,CR, DC, E, EC, pCy,
(1985)
pE, Pi, SK, SM, V
AB, C, BB, BI, BM, BZ,
Panama – PAN Ackerman (1983) 21,842 44 OBS CM, dC, E, G, L, SK, SM,
2pEA, 2pE, V
Costa Rica – CNP – CR1 Janzen et al. (1982) 961 27 IN AB, C, CM, E, SM
Costa Rica – SNRP (300 m) –
Janzen et al. (1982) 720 20 IN AB, C, CM, E, SM
CR2
Costa Rica – SNRP (5 m) – CR3 Janzen et al. (1982) 480 12 IN AB, C, CM, E, SM
1
Method: IN = insect net; BT = baited traps; OBS = identification in the field, without collecting
2
Baits: AA = anisyl acetate; AB = benzyl acetate, AC, cresyl acetate; AlB = benzyl alcohol; BB = benzyl benzoate; BI = β-ionone;
BM = β-myrcene; BZ = methyl benzoate; C = 1,8-cineole or eucalyptol; CM = methyl trans-cinnamate; CR = p -cresol; DB =
dimethoxibenzene; DC = D-cresol methanol; dC = d-carvone; E = eugenol; EC = Ethoxy cinnamate; G = geraniol; L = linalool;
pCy = p -cymere; pE = phenyl ETOH; Pi = piperonol; SK = skatole; SM = methyl salicylate; T = p-tolyl acetate; 2pE = 2-phenyl
ethanol; 2pEA = 2-phenyl ethyl acetate; V = vanillin
3
Thirty nine species were collected, but only the 18 most common species included numbers of specimens, but these represented
at least 98% of the captured bees.878 Nemésio & Silveira - Diversity and Distribution of Orchid Bees (Hymenoptera: Apidae) with a Revised...
(%)
Eg. analis 0 0 0 0 0 0 0.2 0 0 0.3 0 47 0 0 17 0 0 0 5 0 0 0 0 0 0 0 0 0
Eg. chalybeata 0 0 0 0 21 24 9 32 21 21 3 0 1.5 0 0 0 0 0 0 0 2 0 0 0 0 0 0 0
Eg. cordata 0 0 0 0 0 0 0 0 0 0 2 0.2 63 69 44 45 51 15 23 12 4 17 0 0 0.2 0.5 0 0.5
Eg. imperialis 1.7 0.8 24 34 6 11 0.5 2 0.7 0.5 0 0 0 0 7 2 0 0 0 0 3 0 0 0 0.2 0.2 2 0
Eg. pleosticta 0 0 0 0 0 0 0 0 0 0 0 5 0 0 1 0 0 1 2 0 33 52 72 0 27 0.6 0.5 0
Eg. stilbonota 0 0 0 0 0 0 28 53 32 38 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
Eg. viridissima 65 76 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
El. cingulata 1 0.6 8 4 2 1 0.1 0 0.7 0.4 24 20 18 3 3 0 0 22 11 6 2 0 0 4 0 0.5 0.2 0
El. nigrita 1 0.6 8 0.1 0 0 0 0 0 0 0.9 10 8 7 10 49 16 55 28 30 4 10 11 26 28 46 51 1
EMG
SMG
AM4
AM1
AM2
AM3
AM4
MA1
MA3
MA2
PAN
BA1
BA2
RSC
BH1
BH2
CR2
CR3
CR1
PE1
PE2
SP1
SP2
SP3
PB
RS
ES
RJ
100
90
80
70
Percent similarity
60
50
40
30
20
10
0
Fig. 2. Clustering of the 28 sampling sites in the Neotropical Region, according to the similarity of their fauna of Euglossina.
See Table 1 for codes of the areas. Numbers above site acronyms refer to frequencies of the most important species in defining
the groups shown in the dendrograms.
also with low similarity. Lastly, when all Euglossina were regions. This species was recorded in other sites in the states of
considered, the Amazonian Forest clustered first with part São Paulo (SP1, SP2 and SP3), Minas Gerais (EMG, RSC and
of Central America (Panama and the southernmost site of SMG) and Espírito Santo (ES). Nevertheless, its abundance
Costa Rica), then with the Atlantic Forest, and finally with was always below 5% of the total orchid-bee community in all
the two remaining Costa Rican sites. When only species of these areas. The very low frequencies (1% or less) of Euglossa
Euglossa were considered, the Amazonian Forest, including cordata (L.) and Eulaema nigrita Lepeletier, species widely
the Peruvian sites, clustered first with the Atlantic Forest and, distributed in the Neotropics and particularly abundant in the
then, with the Central American region. Atlantic Forest domain, also contributed for the distinction
The orchid bee fauna of the Brazilian state of Rio Grande between Rio Grande do Sul and the Atlantic Forest sites in
do Sul showed almost no similarity with any other area. southeastern and northeastern Brazil.
Thus, in general, there were three distinct groups in South
America (Amazonia, Atlantic Forest, and Subtropical Rain Atlantic Forest domain. With both sets of data (all Euglossina
Forest, the latter represented by Rio Grande do Sul), and one and only species of Euglossa), three subgroups were evident
group for Central America, with two distinct and weakly in the Atlantic Forest areas:
related subgroups (Panama and southwestern Costa Rica,
on one side, and the two northwestern Costa Rican sites, on ● Subgroup 1 (BH1, BH2, RSC, SP1, SP2, SP3, and MA2)
the other). The association among these major groups was constituted mostly by inland, semi-deciduous Atlantic
very weak and will be considered below. Forest in close proximity with the cerrado (Brazilian
savanna). The large frequencies of El. nigrita, Euglossa
Rio Grande do Sul, Brazil. The extremely high frequency of fimbriata Rebêlo & Moure, Euglossa pleosticta Dressler,
Eufriesea violacea (Blanchard) (almost 98% of the bees in and Euglossa truncata Rebêlo & Moure are primarily
the samples) was the main responsible for the dissimilarity responsible for the clustering of these sites. This
between Rio Grande do Sul and the other Atlantic Forest subgroup can be further divided in two clusters: (i) BH1November - December 2007 Neotropical Entomology 36(6) 879
(%)
Eg. analis 0 0 0 0 0 0 0.2 0.3 0 0 0 0 0 0 0 0 0 20 8 0 0 0 0 0 0 0 69
Eg. chalybeata 0 0 0 0 27 27 10 23 36 34 5 2 0 0 0 0 0 0 0 3 0 0 0 0 0 0 0
Eg. cordata 0 0 0 0 0 0 0 0 0 0 3 90 91 82 77 61 54 52 38 5 19 0.3 0 0 1 0 0.2
Eg. fimbriata 0 0 0 0 0 0 0 0 0 0 0.3 0.4 0 0.3 9 37 0 * 1 6 0 39 8 7 27 18 0.6
Eg. imperíalis 2 1 32 47 7 12 0.5 0.6 1 2 0 0 5 0 0 0 0 8 0 4 0 0.3 0 0 1 3 0
Eg. pleosticta 0 0 0 0 0 0 0 0 0 0 0 0 0 0 7 0 0 1 4 42 58 41 88 0 1 1 7
Eg. securigera 0 0 0 0 0 0 0 0 3 0 0 0 0.7 0.7 4 2 0 0.3 12 0.7 0 0.2 0 9 17 7 3
Eg. stilbonota 0 0 0 0 0 0 30 43 48 55 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
Eg. viridissima 76 88 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
EMG
SGM
AM4
AM3
AM2
AM1
MA4
MA1
MA3
MA2
PAN
BA1
BA2
RSC
BH1
BH2
CR2
CR3
CR1
PE1
PE2
SP1
SP3
SP2
PB
ES
RJ
100
90
80
70
Percent similarity
60
50
40
30
20
10
0
Fig. 3. Clustering of 27 areas in the Neotropical region, according to the similarity of their fauna of Euglossa. See Table 1 for
codes of the areas. Numbers above site acronyms refer to frequencies of the most important species in defining the groups shown
in the dendrograms. * = frequencies below 0.05%.
+ BH2 + RSC, which have a high frequency of El. nigrita in five of them (BA2, ES, PB, MA1, and MA3), it was
and Eg. truncata in common, and (ii) SP1 + SP2 + SP3 the dominant orchid-bee species. In some areas (SMG,
(also inland, in the southernmost portion of this cluster) BA1, RJ, PB, and BA2), El. nigrita was very common
+ MA2 (a disturbed forested area in the Amazonian (it was the dominant species in SMG, BA1, and RJ). This
part of Maranhão), where Eg. pleosticta was the most subgroup cannot be clearly divided into clusters, since the
frequent species (33% or more of the specimens). Eg. internal arrangement of its sites greatly changed when all
pleosticta was also the dominant species of Euglossa in Euglossina or only Euglossa were considered (mainly due
SP3 (41%) and, for this reason, this site moved from the to the different frequencies of El. nigrita) (Figs. 2 and 3).
first cluster to the second one when only species of this As Eg. cordata was rare in or absent from the seven areas
genus were considered in the analysis (Fig. 3). However, of Subgroup 1, its frequency seems to be the main factor
as Eg. fimbriata and El. nigrita were present at almost the to separate these two Atlantic Forest subgroups.
same frequencies as Eg. pleosticta in SP3, but in lower
● Subgroup 3 seems to be the result of the incidental
frequencies in the rest of the second cluster, this cluster
grouping of two areas (EMG and MA4) with low
joined the first one when all Euglossina were considered
similarity to each other and with the rest of the Atlantic
(Fig. 2). In the first cluster (Belo Horizonte region),
Forest areas. In fact, these areas were grouped only when
Eg. pleosticta does occur, but in very low frequencies
one considers all Euglossina (Fig. 2), since Eulaema
(Nemésio & Silveira 2007).
cingulata (Fabricius) was responsible for most of the
● Subgroup 2 (BA1, BA2, MA1, MA2, SMG, PB, ES similarity between these two areas. When only species
and RJ) is represented mostly by coastal forest. The of Euglossa were considered, MA4 grouped with the
exception is SMG, which, notwithstanding, is closer to Amazonian areas (Fig. 3). The dominant species in
the coast than the other areas in Minas Gerais clustered MA4 was Euglossa piliventris Guérin-Méneville, which
in Subgroup 1 (BH1, BH2 and RSC). Eg. cordata was occur only in low frequencies in MA2, MA3, and AM3.
the dominant Euglossa species in all these areas and, EMG represented a singular fauna within the Atlantic880 Nemésio & Silveira - Diversity and Distribution of Orchid Bees (Hymenoptera: Apidae) with a Revised...
Forest fragments. There, the dominant species was hundred and seven species of five genera of Euglossina are
Euglossa analis Westwood (47% of all Euglossina), a currently recognized (see Appendix 1), one species in Aglae
species that was also relatively abundant in ES (17%) Lepeletier & Serville, seven in Exaerete Hoffmannsegg, 27
and that occurred in lower frequencies in RJ (5%) and in Eulaema Lepeletier, 65 in Eufriesea, and 107 in Euglossa.
in some Amazonian areas (AM3 and AM4 – less than Two of these species are only known as fossil specimens
1%). EMG showed a moderate similarity to RJ (36%) preserved in Dominican amber (Engel, 1999): Eufriesea
and ES (33%), which are relatively close in the same melissiflora (Poinar) and Euglossa moronei Engel. Moreover,
domain (see Fig. 1). Moreover, EMG and ES are part of two undescribed species of Eufriesea (Schwartz Filho &
the same hydrographic basin. Eg. cordata was present Laroca 1999, D. Yanega, pers. comm.) and two of Euglossa
in high frequencies in these two latter areas (44% of all (Bembé 2004) have been recognized but have not been
Euglossina in ES and 23% in RJ) and was responsible published yet. So, the total number of orchid bee species
for clustering them in Subgroup 1. In contrast, in EMG reaches, at least, 210 species.
this species represented only 0.2% of the orchid bees. The Amazon Basin is the area with the highest number of
species — 127. In Central America, 76 species of orchid bees
Amazonian Forest domain. [AM1, AM2, AM3, AM4, were recorded and 62 species were recorded in the Atlantic
PE1 and PE2 (AM4 = canopy; PE1 = floodplain; PE2 = Forest (Appendix 1). The endemism is also highest in the
Terra Firme)]. Brazilian (central-eastern Amazonia) and Amazon Basin — 77 species. In Central America 40 extant
Peruvian (western Amazonia) areas shared several species endemic species are found, whereas 27 orchid-bee species
with Euglossa chalybeata Friese, the only present in high are endemic to the Atlantic Forest.
frequencies in both regions, as the main responsible for
joining them. The Brazilian areas clustered in a separate
group because they share a dominant species (28% - 53% of Discussion
all orchid bees), Euglossa stilbonota Dressler, which was not
recorded in the Peruvian areas. On the other hand, Euglossa Distribution and diversity. Dendrograms resulting from
ignita Smith and Eg. chalybeata are the dominant species in cluster analyses do not necessarily bear any phylogenetic
the Peruvian Amazon, with frequencies varying between 21% or historical information. However, the main biogeographic
and 27% of all Euglossina. Both species are present in the regions suggested by our analyses are much coincident
Brazilian Amazon, the former in low frequencies, while the with biogeographic components identified on basis of
latter was the second most common species and accounted phylogenetic analyses of other bee groups, flies (Diptera) and
for ca. 25% of all Euglossina. primates (Camargo 1996, Amorim & Pires 1996).
It must be emphasized that all sites sampled in the These papers suggested an ancient division of South
Brazilian Amazon are in the same area, ca. 90 km north of America in a northwestern, mainly Amazonic, component
Manaus. Thus, the high similarity among these sites was and a southeastern one, including the southeastern limits of
expected. On the other hand, it is interesting to note that the Amazonia, the Atlantic Forest, the cerrado and the caatinga.
canopy fauna (AM4) was the most distinctive among the These papers also suggested divisions of the northwestern
ones in the Brazilian Amazonian sites, sharing only about component in three sub-components – (i) a basal one
50% similarity with them. composed by the northern pacific coast of South America plus
Central America; (ii) a southwestern Amazonic region and (iii)
Central America. The four Central American sites were a northeastern Amazonic region. Moreover, area cladograms
divided into two subgroups, which were weakly related to obtained by Camargo (1996) and Camargo & Pedro (2003),
each other: Panama (PAN) and Corcovado National Park, based on the phylogenies of three genera of meliponine bees,
southwestern Costa Rica (CR1), in one cluster, and the two suggest the existence of a coastal and an interior region in
areas in Parque Nacional Santa Rosa, northwestern Costa the Atlantic Forest component, what is coincident with data
Rica (uplands, CR2 and lowlands, CR3), in the other. They presented in this paper. Although relation between specific
were in the same cluster when only species of Euglossa were geological events and these biogeographic divisions were
considered (Fig. 3). Euglossa tridentata Moure (26%) and not confidently established yet, the coincidence of results
Euglossa imperialis Cockerell (24%) were the most common obtained from such diverse group of animals suggests these
species in Panama. This latter species was dominant at CR1 biogeographic regions to be real historic entities. It seems,
(34%) and occurred in very low numbers in northwestern thus, that the regions indicated by the analyses presented here
Costa Rican sites, but these two species were primarily also coincide with historical biogeographic units.
responsible for clustering these areas together, with a very low It is surprising that historic units as close as the interior and
similarity index (ca. 6% - Fig. 3). When all Euglossina were coastal regions of the Atlantic Forest still can be distinguished
considered, CR2 and CR3 form an isolate branch that unites through the analysis of data from a group of powerful flyers
to a large group formed by the Atlantic Forest + (Amazonian such as the orchid bees, which might be expected to easily
Forest + PAN and CR1) (Fig. 2). This occurred because disperse along the whole domain. This is probably due the
Euglossa viridissima Friese was by far the most common ecological differences between the evergreen rainy forests
species at both sites in northwestern Costa Rica (65% in CR2 of the coast and the semi-deciduous seasonal forests in the
and 76% in CR3), but was absent from all other sites. interior. Bees in the interior areas inhabit forests with lower
canopies and with understories more exposed to sunlight and
Richness and endemism along the Neotropical Region. Two wind than those near the coast (Rizzini 1979).November - December 2007 Neotropical Entomology 36(6) 881
Although many euglossine species do have wide Geographically speaking, Maranhão is much closer to the
geographic ranges, many of them are very restrictive in Amazonian domain than to the region currently covered by
respect to the kind of environment they inhabit in nature. the Atlantic Forest. Nevertheless, when the biogeographic
Thus, some of them, such as Eg. analis and El. niveofasciata areas recognized by Amorim & Pires (1996), Camargo (1996)
(Friese), are only found in the very interior of humid, close- and Camargo & Pedro (2003) are considered, the state is on
canopy forests and are unable to cross narrow bands of the boundary between the northwestern and the southeastern
deforested land (Powell & Powell 1987). Others, such as South American components.
El. nigrita and Eg. cordata, on the other hand, seem to be Historically, it has been suggested that connections
best adapted to drier, illuminated environments (e.g. Morato between the Amazonian and the Atlantic Forests existed in
et al. 1992, Silva & Rebêlo 2002, Tonhasca Jr. et al. 2002, the near past, until Europeans reached South America (e.g.
Nemésio 2004). It should be noted that many of these latter Coimbra-Filho & Câmara 1996). If this is true, the coastal
species are the same found in the cerrado (Nemésio & Faria region of Maranhão was probably part of the transition zone
Jr. 2004), the savannic vegetation that covers central Brazil. between those biomes, and the current composition of its
This suggests that the cerrado and the Atlantic Forest would euglossine fauna is just a testimony of this. Ecologically, the
have clustered together, if data from the former domain were fragmentation and disturbance of the Amazonian forests in
available for our analyses, as the southeastern biogeographic Maranhão may have allowed for their recently colonization
component of South America devised by Amorim & Pires by species such as El. nigrita and Eg. cordata. These species,
(1996), Camargo (1996) and Camargo & Pedro (2003). which are the main responsible for clustering areas of
A few odd positionings of specific sites or regions in the Maranhão with those in the Atlantic Forest, seem to be well
dendrogram deserve some discussion. Thus, the Brazilian adapted to open and/or disturbed areas, as indicated above.
state of Rio Grande do Sul appears as a distinctive branch at Generally speaking, the two main regions devised in the
the base of the dendrograms, isolated from all other sampling Amazonian region (western, in Peru, and Central, in Brazil)
sites. However, this region would be expected to cluster with correspond to the two main subdivisions of the northwestern
other sites in Atlantic Forest domain. It could be argued that biogeographic component of South America, as suggested by
this region was sampled only during the summer months, the Amorim & Pires (1996), Camargo (1996) and Camargo &
only season when adult Eufriesa are active (Kimsey 1982). Pedro (2003). This region, however, is very badly sampled.
The high abundance of Ef. violacea in that region, which In our analyses, it was represented by two sets of sites
made it so dissimilar to all other sites, could, then, represent from two restricted areas. For a better understanding of
an overestimation of its actual frequency. Nonetheless, even the relationships among the local Amazonian faunas, more
overestimated, the abundance of Ef. violacea in Rio Grande areas must be sampled in different regions of that domain.
do Sul was surprisingly high since, in other places, species of Additional sampling in areas in southeastern Amazonia
this genus are always captured in low numbers, never above (southern state of Pará and northern state of Tocantins),
5% of the individuals (e.g. Rebêlo & Garófalo 1991, 1997, southwestern Amazonia (Brazilian states of Acre and
Peruquetti et al. 1999, Nemésio 2004). This led authors to Rondonia and north of Mato Grosso) as well as in northern
generally consider species of Eufriesea as rare (e.g. Kimsey South America (Colombia, Venezuela) and on the western
1982, Nemésio & Silveira 2004, Nemésio 2005a). Andean slopes are important to test the concordance of
Furthermore, samplings in the intervening region similarity patterns with historic patterns in euglossine faunas
between Rio Grande do Sul and other sites in the Atlantic in northern South America.
Forest (southern São Paulo and the states of Paraná and The sharp differences between the northwestern Costa
Santa Catarina) were not available when our analyses were Rican sites and the southwestern area + Panama should not
carried on. Samplings in these areas could have made the be ignored and wait for an explanation. The species list of
transition between Rio Grande do Sul and the other sites in Colombian orchid bees (Bonilla-Gómez & Nates-Parra 1992)
the Atlantic Forest smoother than that shown in Fig. 2. This suggests that, if data on local faunas were available for this
is supported by results published recently by Sofia & Suzuki country, they might have acted as a link between southern
(2004) and Sofia et al. (2004) for northern Paraná state. In Central America and the Amazon Forest, eventually placing
this region, frequencies of Ef. violacea ranged from 33% to Amazonia closer to Central America than to the Atlantic
50%. On the other hand, the number of species found by these Forest, as suggested by the phylogeny-based analyses of
authors was also higher than that observed in Rio Grande do Amorim & Pires (1996), Camargo (1996) and Camargo
Sul and included larger frequencies of some species, such & Pedro (2003). A closer relationship between orchid bee
as El. nigrita, Eg. pleosticta and Eg. fimbriata, which are faunas of Central America and the northern Pacific coast of
particularly common in other sites of the Atlantic Forest. South America and Central America, as suggested by the area
These works by Sofia and colleagues, published when our cladograms of Amorim & Pires (1996), Camargo (1996) and
paper was under review, fit the kind of transition we would Camargo & Pedro (2003), can also be antecipated from the
expect to find in Paraná and Santa Catarina. Otherwise, the results of Dick et al. (2004), which indicated the Andes as an
impoverishment of the euglossine fauna toward southern effective barrier for the gene flow between populations on its
South America, already shown by Rebêlo (2001), just fits eastern and western slopes. Whether or not this will show to be
the well-recognized general trend of decreasing diversity true depends on the proportion of speciation events that have
associated to increasing latitude (e.g. Begon et al. 1986). occurred after the uplift of the Andes. According to Camargo
The fluctuation of the sampling sites in Maranhão among (1996) and Dick et al. (2004), most of them occurred recently,
the Amazonian and Atlantic Forest sites also calls attention. in response to climatic and environmental changes.882 Nemésio & Silveira - Diversity and Distribution of Orchid Bees (Hymenoptera: Apidae) with a Revised...
It should be kept in mind that part of the heterogeneity fragmentation of this biome occurred. Although many species
found among sites inside each of the geographic regions are currently threatened by extinction (Birdlife International
recognized here may be due to human activity. Fragmentation 2000), only two bird species [Cyanopsitta spixii (Wagler)
and disturbance of natural vegetation may have lead to the and Mitu mitu (L.)] did become extinct (and only recently)
reduction (some times extinction) of local populations of in the wild (see Nemésio 2001). All other species remain and
some species and to the increasing (sometimes invasion) of most of them are still found in the same areas where earlier
the populations of other species in specific sites. Thus, for a naturalists found them (Sick 1997, Tobias et al. 2006), in spite
reliable picture of orchid bee biogeography to be constructed, of deforestation. Thus, we may suppose that extinction was
it is urgent that areas suffering high deforastation rates, such probably not high among orchid bees. If this is true, then,
as the southern portion of the state of Pará or the state of contrary to what seems to be true for other taxa, the Atlantic
Rondônia (both in Brazil), are sampled. Forest is not a hotspot (Mittermeier 1999) for orchid bees.
Most of the species listed as endemic to this domain are
Endemism and richness variation among regions. tolerant to open areas or to high elevations.
Peruquetti et al. (1999, p.107) suggested that the species Eulaema seabrai Moure, which has been treated as a
richness of Euglossina in the Atlantic Forest domain was species typical of dense forest (Dressler 1979, Oliveira
higher than that of the Central Amazon. The analysis of the 2000) was recently collected in an urban area close to Belo
data in the Appendix suggests otherwise. One problem is Horizonte (Nemésio & Silveira 2004). Among the most
that they compared a list of every species ever collected in common orchid bees listed as endemic in Appendix 1, only El.
the whole Atlantic Forest domain to the species collected in flavescens (Friese) seems to be exclusively associated to the
a few specific sites, all in the same region of the Amazon typical coastal Atlantic Rain Forest. It should be emphasized,
Basin, during one-year samplings. Moreover, they included, however, that the Atlantic Forest is not a homogeneous domain
among the 57 species they assigned to the Atlantic Forest concerning orchid bee fauna. Some species, as the recently
domain, two unidentified species of Eufriesea and four of described Euglossa anodorhynchi Nemésio, are restricted to
Euglossa, which are not known to be different from each southern Brazil (Nemésio 2006) and other ones, such as Eg.
other or from other species already present on their list. mandibularis Friese and Ef. violacea are distributed from
Also, Euglossa chalybeata iopoecila Dressler, Eulaema southern to southeastern Brazil. Other species, such as El.
bombiformis niveofasciata (Friese), and Eulaema meriana flavescens, El. niveofasciata, Eg. cyanochlora Moure, are
flavescens (Friese) are there listed as subspecies. restricted to areas ranging from Paraíba, in northeastern Brazil,
When lists of all species ever collected in Central America to Espírito Santo and Rio de Janeiro in the east.
and in the Amazon Basin are compared to the complete list of On the other hand, the euglossine fauna of Amazonia seems
species from the Atlantic Forest, the latter presents the poorest to be composed of a high number of species intolerant to open
orchid bee fauna among the three geographic areas compared, and/or disturbed habitats (Morato 1994), some of which fail to
even when species that are not strictly endemic to this biome cross only a few dozen meters of open space between forest
are included. Examples of the latter are Euglossa melanotricha fragments (Powell & Powell 1987). A remarkable difference
Moure, Eg. truncata, Eg. securigera Dressler, and Eg. between the Amazonian and the Atlantic Forest faunas (and,
fimbriata which are present in the cerrado (Brazilian savanna to a lesser extent, the Central American fauna) is the low
– Nemésio & Faria Jr. 2004). Nevertheless, as discussed frequencies of species of Eulaema in the former, although
before, the Atlantic Forest and the cerrado seem to be part of a the Amazon Forest and northern South America present the
single major southeastern biogeographic component of South highest number of species in this genus (Oliveira 2000). In the
America (Amorim & Pires 1996, Camargo 1996, Camargo & Atlantic Forest, El. nigrita and, to a lower degree, El. cingulata
Pedro 2003). This suggests a close historic relationship and are among the most common species (in all the 13 areas of
not simple dispersion and/or interchange of faunistic elements Atlantic Forest, El. nigrita is one of the most common species
between these two seasonal semi-deciduous domains. and in three areas El. cingulata is also common). In contrast, no
The degree of endemism in the Atlantic Forest is also the species of Eulaema figures among the most common species in
lowest of all three regions. It is difficult to determine whether the Amazonian areas and only in southern Costa Rica, among
the low orchid bee endemism in the Atlantic Forest is an the Central American sites, does the frequency of El. meriana
actual characteristic of the biome or whether it is the result (Olivier) reach 14% of all orchid bees. As the Atlantic Forest,
of five centuries of fragmentation. After all, orchid bees are the Amazon Basin is far from homogeneous concerning the
not easily caught without the aid of the attractive compounds orchid bee fauna. Although several species are widespread,
which were discovered only in the 1960’s (Dodson et al. some are restricted to limited regions of the domain. For
1969) and all the scarce records of orchid bees (mostly of example, Eg. stilbonota and Eg. piliventris have only been
female specimens) prior to that date were fortuitous. Since collected in eastern Amazonia, whereas Eg. rugilabris Moure,
it is impossible to know how much of the original fauna of Eg. lugubris Roubik, and Eg. occidentalis Roubik are restricted
the Atlantic Forest was sampled, it may be useful to look at to western Amazonia (see Roubik 2004).
what is known from other taxa, such as birds. The differences between the species composition of the
The comparison with birds seems reasonable, since orchid Amazonian areas and of the Central American ones are also
bees are known for their remarkable flight capability and outstanding. The Amazonian forest shares more species with
because them, as birds but contrary to other bees, are most the Atlantic Forest than with Central America (Appendix 1).
diverse and abundant in tropical forests (Michener 1990). Two explanations are possible: (i) the data reflect the original
For birds, good estimates were made before most of the community composition of the Amazonian and CentralNovember - December 2007 Neotropical Entomology 36(6) 883
American biotas, each with a high level of endemism, or Brito, C.M.S. & M.M.C. Rêgo. 2001. Community of male
(ii), the observed similarities are due to poor sampling of Euglossini bees (Hymenoptera: Apidae) in a secondary forest,
vast Amazonian areas, especially in its northern portion. This Alcântara, MA, Brazil. Braz. J. Biol. 61: 631-638.
second hypothesis is supported by the fact that most Central Camargo, J.M.F. 1996. Meliponini neotropicais (Apinae, Apidae,
American “endemic” species reach northern Colombia Hymenoptera): biogeografia histórica. Anais do Encontro sobre
(Bonilla-Gómez & Nates-Parra 1991) and might also be Abelhas 2: 107-121.
present in the subsampled Amazonian areas of Venezuela,
Colombia, and northern Brazil. Most species of Amazonian Camargo, J.M.F. & S.R.M. Pedro. 2003. Meliponini neotropicais:
birds, a well sampled taxon in the area, are also present in O gênero Partamona Schwarz, 1939 (Hymenoptera, Apidae,
Central America (Ridgely & Tudor 1989, 1994), and a similar Apinae) – bionomia e biogeografia. Revta. Bras. Entomol.
pattern may be obtained for orchid bees after these areas are 47: 311-372.
better sampled. It is then necessary to consider that sampling Coimbra-Filho, A.F. & L.G. Câmara. 1996. Os limites originais do
orchid bees to answer the questions posed above is an urgent bioma Mata Atlântica na região norte do Brasil. Rio de Janeiro,
task, since the fast destruction of native vegetation throughout Fundação Brasileira para a Conservação da Natureza, 86p.
their ranges may create artificial gaps in the geographic
distribution of the involved species. Dick, C.W., D.W. Roubik, K.F. Gruber & E. Bermingham. 2004. Long-
distance gene flow and cross-Andean dispersal of lowland rainforest
bees (Apidae: Euglossini) revealed by comparative mitochondrial
Acknowledgements DNA phylogeography. Mol. Ecol. 13: 3775–3785.
Dodson, C.H., R.L. Dressler, H.G. Hills, R.M. Adams & N.H.
To Jacquelyn L. Blackmer for her careful reading of this Williams. 1969. Biologically active compounds in orchid
manuscript. Three anonymous referees greatly contributed fragrances. Science 164: 1243-1249.
to improve this work.
Dressler, R.L. 1979. Eulaema bombiformis, E. meriana, and
Müllerian mimicry in related species (Hymenoptera: Apidae).
References Biotropica 11: 144-151.
Dressler, R.L. 1982. Biology of the orchid bees (Euglossini). Ann.
Ackerman, J.D. 1983. Diversity and seasonality of male euglossine bees Rev. Ecol. Syst. 13: 373-394.
(Hymenoptera: Apidae) in central Panamá. Ecology 64: 274-283.
Engel, M.S. 1999. The first fossil Euglossa and phylogeny of the
Amorim, D.S. & M.R.S. Pires. 1996. Neotropical biogeography orchid bees (Hymenoptera: Apidae; Euglossini). Am. Mus.
and a method for maximum biodiversity estimation, p.183- Novitates 3272: 1-14.
219. In C.E.M. Bicudo & N.A. Menezes (eds.), Proceedings
of the Workshop Methods for the Assessment of Biodivesity Janzen, D.H., P.J. Devries, M.L. Heggins & L.S. Kimsey. 1982.
in Plants and Animals. Brasília, CNPq. Seasonal and site variation in Costa Rican euglossine bees at
chemical baits in lowland deciduous and evergreen forests.
Becker, P., J.S. Moure & F.J.A. Peralta. 1991. More about euglossine Ecology 63: 66-74.
bees in Amazonian forest fragments. Biotropica 23: 586-591.
Kimsey, L.S. 1982. Systematics of bees of the genus Eufriesea.
Begon, M., J.L. Harper & C.R. Townsend. 1986. Ecology – individuals, Univ. California Publ. Entomol. 95: 1-97.
populations, and communities. Blackwell, Oxford, 876p.
Kimsey, L.S. & R.L. Dressler. 1986. Synonymic species list of
Bembé, B. 2004. Revision der Euglossa cordata-Gruppe und Euglossini. Pan-Pacific Entomol. 62: 229-236.
Untersuchungen zur Funktionsmorphologie und Faunistic der
Euglossini (Hymenoptera, Apidae). D. S. thesis. München, Lyons, S.K. & M.R. Willig. 2002. Species richness, latitude, and
Ludwig-Maximilians-Universität München, 177 p. scale-sensitivity. Ecology 83: 47-58.
Bezerra, C.P. & C.F. Martins. 2001. Diversidade de Euglossinae Michener, C. 1990. Classification of the Apidae. Univ. Kansas Sci.
(Hymenoptera, Apidae) em dois fragmentos de Mata Atlântica Bull. 54: 5-164.
localizados na região urbana de João Pessoa, Paraíba, Brasil. Mittermeier, R.A., N. Myers, P. Roblesgil & C. Goetisch-
Revta. Bras. Zool. 18: 823-835. Mittermeier. 1999. Hotspots. Mexico, CEMEX, 430p.
BirdLife International 2000. Threatened birds of the world. Morato, E.F. 1994. Abundância e riqueza de machos de Euglossini
Barcelona, Lynx Edicions and BirdLife International, 852p. (Hymenoptera: Apidae) em mata de terra firme e áreas de
Bonilla-Gómez, M.A. 1999. Caracterização da estrutura espaço- derrubada, nas vizinhanças de Manaus (Brasil). Bol. Mus. Par.
temporal da comunidade de abelhas euglossinas (Hymenoptera, Emílio Goeldi, série Zool.10: 95-105.
Apidae) na Hiléia Bahiana. Tese de doutorado, Universidade Morato, E.F. 1998. Estudos sobre comunidades de abelhas
Estadual de Campinas, Campinas. xii + 153p. Euglossini. Anais do Encontro sobre Abelhas 3: 135-143.
Bonilla-Gómez, M.A. & G. Nates-Parra. 1991. Abejas euglosinas Morato, E.F., L.A.O. Campos & J.S. Moure 1992. Abelhas
de Colombia (Hymenoptera: Apidae) I. Claves ilustradas. Euglossini (Hymenoptera, Apidae) coletadas na Amazônia
Caldasia 17: 149-172. Central. Revta. Bras. Entomol. 36: 767-771.884 Nemésio & Silveira - Diversity and Distribution of Orchid Bees (Hymenoptera: Apidae) with a Revised...
Moure, J.S. 1967. A check-list of the known euglossine bees Neves, E.L. & B.F. Viana. 1997. Inventário da fauna de Euglossinae
(Hymenoptera, Apidae). Atas Simp. Biota Amaz. 5(Zool.): (Hymenoptera: Apidae) do baixo sul da Bahia, Brasil. Revta
395-415. Bras. Zool. 14: 831-837.
Moure, J.S. 1999. Novas espécies e notas sobre Euglossinae do Neves, E.L. & B.F. Viana. 1999. Comunidade de machos de
Brasil e Venezuela (Hymenoptera, Apidae). Revta Bras. Zool. Euglossinae (Hymenoptera: Apidae) das matas ciliares da
16(Suppl. 1): 91-104. margem esquerda do Médio Rio São Francisco, Bahia. An.
Soc. Entomol. Brasil 28: 201-210.
Moure, J.S. 2003 [2000]. As espécies do gênero Eulaema Lepeletier,
1841 (Hymenoptera, Apidae, Euglossinae). Acta Biol. Par. Oliveira, M.L. 2000. O gênero Eulaema Lepeletier, 1841
29: 1-70. (Hymenoptera, Apidae, Euglossini): Filogenia, biogeografia
e relações com as Orchidaceae. Tese de Doutorado. Ribeirão
Nemésio, A. 2001. The extinction of Spix’s Macaw in the wild. Preto, Universidade de São Paulo, 159p.
World Birdwatch 23: 9-11.
Oliveira, M.L. 2006a. Três novas espécies de abelhas da Amazônia
Nemésio, A. 2004. Composição e riqueza em espécies e abundância pertencentes ao gênero Eulaema (Hymenoptera: Apidae:
de machos de Euglossina (Hymenoptera: Apidae: Apini) de Euglossini). Acta Amazonica 36: 121-128.
remanescentes florestais de Mata Atlântica no estado de Minas
Gerais. Dissertação de Mestrado. Universidade Federal de Oliveira, M.L. 2006b. Nova hipótese de relaciofamento filogenético
Minas Gerais, Belo Horizonte. xii + 153p. entre os gêneros de Euglossini e entre as espécies de Eulaema
Lepeletier, 1841 (Hymenoptera: Apidae: Euglossini). Acta
Nemésio, A. 2005a. Description of the male Eufriesea nigrohirta Amazonica 36: 273-286.
(Friese, 1899) (Hymenoptera: Apidae: Euglossina) with
comments on the holotype, species biology and distribution. Oliveira, M.L. & L.A.O. Campos. 1996. Preferências por estratos
Lundiana 6: 41-45. florestais e por substâncias odoríferas em abelhas Euglossinae
(Hymenoptera, Apidae). Revta Bras. Zool. 13: 1075-1085.
Nemésio, A. 2005b. Fluorescent colors in orchid bees (Hymenoptera:
Apidae). Neotrop. Entomol. 34: 933-936. Pearson, D.L. & R.L. Dressler. 1985. Two-year study of male orchid
bee (Hymenoptera: Apidae: Euglossini) attraction to chemical
Nemésio, A. 2005c. Orchid bees (Hymenoptera: Apidae: baits in lowland south-eastern Peru. J. Trop. Ecol. 1: 37-54.
Euglossina) of Ilha de Maracá, Roraima, northern Brazil.
Lundiana 6: 117-119 Peruquetti, R.C., L.A.O. Campos, C.D.P. Coelho, C.V.M. Abrantes
& L.C.O. Lisboa. 1999. Abelhas Euglossini (Apidae) de áreas
Nemésio, A. 2006. Euglossa anodorhynchi sp. n. (Hymenoptera: de Mata Atlântica: Abundância, riqueza e aspectos biológicos.
Apidae), a new orchid bee from southern Brazil. Neotrop. Revta. Bras. Zool. 16 (Supl. 2): 101-118.
Entomol. 35: 206-209.
Powell, A.H. & G.V.N. Powell. 1987. Population dynamics of male
Nemésio, A. & L.R.R. Faria Jr. 2004. First assessment of orchid euglossine bees in Amazonian forest fragments. Biotropica
bee fauna (Hymenoptera: Apidae: Apini: Euglossina) of Parque 19: 176-179.
Estadual do Rio Preto, a cerrado area in southeastern Brazil.
Ramírez, S., R.L. Dressler & M. Ospina. 2002. Abejas Euglosinas
Lundiana 5: 113-117.
(Hymenoptera: Apidae) de la Región Neotropical: Listado
Nemésio, A. & E.F. Morato. 2004. Euglossina (Hymenoptera: de espécies com notas sobre su biología. Biota Colombiana
Apidae: Apini) of the Humaitá Reserve, Acre state, Brazilian 3: 7-118.
Amazon, with comments on bait trap efficiency. Revta Tecnol.
Rebêlo, J.M.M. 2001. História natural das euglossíneas, as abelhas
Amb. 10: 71-80.
das orquídeas. São Luís, Lithograph.
Nemésio, A. & E.F. Morato. 2006. The orchid-bee fauna
Rebêlo, J.M.M. & A.J.M. Cabral. 1997. Abelhas Euglossinae de
(Hymenoptera: Apidae) of Acre state (northwestern Brazil)
Barreirinhas, zona do litoral da baixada oriental maranhense.
and a re-evaluation of euglossine bait-trapping. Lundiana 7:
Acta Amazonica 27: 145-152.
59-64.
Rebêlo, J.M.M. & C.A. Garófalo. 1991. Diversidade e sazonalidade
Nemésio, A. & F.A. Silveira. 2004. Biogeographic notes on rare
de machos de Euglossini (Hymenoptera, Apidae) e preferência
species of Euglossina (Hymenoptera: Apidae: Apini) occurring
por iscas odores em um fragmento de floresta no Sudeste do
in the Brazilian Atlantic Rain Forest. Neotrop. Entomol. 33:
Brasil. Revta Bras. Biol. 51: 787-799.
117-120.
Rebêlo, J.M.M. & C.A. Garófalo. 1997. Comunidades de Machos
Nemésio, A. & F.A. Silveira. 2006. Edge effects on the orchid-bee
de Euglossini (Hymenoptera: Apidae) em matas semidecíduas
fauna (Hymenoptera: Apidae) at a large remnant of Atlantic
do nordeste do estado de São Paulo. An. Soc. Entomol. Brasil.
Rain Forest in southeastern Brazil. Neotrop. Entomol. 35:
26: 243-255.
313-323.
Ridgely, R.S. & G. Tudor. 1989. The birds of South America. Vol.
Nemésio, A. & F.A. Silveira. 2007. Euglossine bee fauna
I. Austin, Austin University of Texas Press, 519p.
(Hymenoptera: Apidae: Euglossina) of Atlantic Forest
fragments inside an urban area in southeastern Brazil. Neotrop. Ridgely, R.S. & G. Tudor. 1994. The birds of South America. Vol.
Entomol. 36: 186-191. II. Austin, Austin University of Texas Press, 814p.You can also read
